Deep marine biosphere fuelled by increasing organic matter availability during burial and heating

Deep marine biosphere fuelled by increasing organic matter availability during burial and heating


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ABSTRACT Deep-sea sediments become apparently more hostile to life with increasing depth as temperature and pressure rise, and organic matter becomes increasingly recalcitrant.


Demonstrations of high bacterial populations in deep sediments1,2 may thus appear enigmatic. How, then, can the continued presence of active bacterial populations in deep sediments that are


over 10 million years old be explained? Although volatile fatty acids, particularly acetate, are important intermediates in the anaerobic degradation of organic matter3,4, their


concentrations are kept very low in sediments (<15 µM) by rapid bacterial consumption5,6. Here we show that heating surface coastal marine sediments to simulate increasing temperature


during burial produces an increase of over three orders of magnitude in acetate concentration and increases bacterial activity. We found that pore-water acetate concentration at two sites in


the Atlantic Ocean increased at depths below about 150 m and was associated with a significant stimulation in bacterial activity. Comparing these acetate concentrations to _in situ_


temperatures confirmed that there was a notable generation of acetate associated with temperature increases during burial. This was supported by heating experiments with deep sediments.


Thus, acetate generation from organic matter during burial may explain the presence of a deep bacterial biosphere in marine sediments, and could underpin an even deeper and hotter biosphere


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Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS END-PERMIAN MARINE EXTINCTION DUE TO TEMPERATURE-DRIVEN NUTRIENT RECYCLING AND EUXINIA Article 28 October 2021


HADAL TRENCHES ARE DYNAMIC HOTSPOTS FOR EARLY DIAGENESIS IN THE DEEP SEA Article Open access 29 January 2021 INACTIVE HYDROTHERMAL VENT MICROBIAL COMMUNITIES ARE IMPORTANT CONTRIBUTORS TO


DEEP OCEAN PRIMARY PRODUCTIVITY Article 29 January 2024 REFERENCES * Parkes, R. J._et al_. Deep bacterial biosphere in Pacific Ocean sediments. _Nature_ 371, 410–413 (1994). Article  ADS 


Google Scholar  * Cragg, B. A._et al_. Bacterial populations and processes in sediments containing gas hydrates (ODP Leg 146: Cascadia Margin). _Earth Planet. Sci. Lett._ 139, 497–507


(1996). Article  ADS  CAS  Google Scholar  * Sørensen, J., Christensen, D. & Jørgensen, B. B. Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic


marine sediment. _Appl. Environ. Microbiol._ 42, 5–11 (1981). PubMed  PubMed Central  Google Scholar  * Winfrey, M. R. & Ward, D. M. Substrates for sulfate reduction and methane


production in intertidal sediments. _Appl. Environ. Microbiol._ 45, 193–199 (1983).] CAS  PubMed  PubMed Central  Google Scholar  * Jørgensen, B. B. Mineralisation of organic matter in the


sea bed: The role of sulphate reduction. _Nature_ 296, 643–645 (1982). Article  ADS  Google Scholar  * Wellsbury, P. & Parkes, R. J. Acetate bioavailability and turnover in an estuarine


sediment. _FEMS Microbiol. Ecol._ 17, 85–94 (1995). Article  CAS  Google Scholar  * Whiticar, M. J., Faber, E. & Schoell, M. Biogenic methane formation in marine and freshwater


environments: CO2 reduction vs. acetate fermentation: Isotope evidence. _Geochim. Cosmochim. Acta_ 50, 693–709 (1986). Article  ADS  CAS  Google Scholar  * Cooles, G. P., Mackenzie, A. S.


& Parkes, R. J. Non-hydrocarbons of significance in petroleum exploration: Volatile fatty acids and non-hydrocarbon gases. _Mineral. Mag._ 51, 483–493 (1987). Article  CAS  Google


Scholar  * Borgund, A. E. & Barth, T. Generation of short-chain organic-acids from crude-oil by hydrous pyrolysis. _Org. Geochem._ 21, 943–952 (1994). Article  CAS  Google Scholar  *


Whelan, J. K._et al_. Evidence for sulfate-reducing and methane-producing organisms in sediments from Sites 618, 619 and 622. _Init. Rep. Deep-Sea Drill. Proj._ 96, 767–775 (1986). CAS 


Google Scholar  * King, G. M. Measurement of acetate concentrations in marine pore water by using an enzymatic approach. _Appl. Environ. Microbiol._ 57, 3476–3481 (1991). CAS  PubMed  PubMed


Central  Google Scholar  * Dickens, G. R._et al_. Direct measurements of _in situ_ methane quantities in a large gas-hydrate reservoir. _Nature_ 385, 426–428 (1997). Article  ADS  CAS 


Google Scholar  * Cragg, B. A._et al_. Bacterial biomass and activity profiles within deep sediment layers. _Proc. ODP Sci. Res._ 112, 607–619 (1990). CAS  Google Scholar  * Wellsbury, P.,


Herbert, R. A. & Parkes, R. J. Bacterial activity and production in near-surface estuarine and freshwater sediments. _FEMS Microbiol. Ecol._ 19, 203–214 (1996). Article  CAS  Google


Scholar  * Paull, C. K._et al_. Leg 164—gas hydrate sampling on the Blake Ridge and Carolina Rise. _Proc. ODP Init. Rep._ 164, 623 ((1966)). Google Scholar  * Barth, T. Quantitative


determination of volatile carboxylic acids in formation water by isotachophoresis. _Anal. Chem._ 59, 2232–2237 (1987). Article  CAS  Google Scholar  * Stetter, K. O. Hyperthermophiles in the


history of life. _Ciba Found. Symp._ 202, 1–18 (1996). CAS  PubMed  Google Scholar  * Cragg, B. A. & Parkes, R. J. Bacterial profiles in hydrothermally active deep sediment layers from


Middle Valley (N.E. Pacific) Sites 857 and 858. _Proc. ODP Sci. Res._ 139, 509–516 (1993). Google Scholar  * Haridon, S. L., Reysenbach, A., Glenat, P., Prieur, D. & Jeanthon, C. Hot


subterranean biosphere in continental oil reservoir. _Nature_ 377, 223–224 (1995). Article  ADS  Google Scholar  * Galimov, E. M. & Kvenvolden, K. A. Concentrations and carbon isotopic


compositions of CH4 and CO2 in gas from sediments of the Blake Outer Ridge, Deep-Sea Drilling Project Leg 76. _Init. Rep. Deep-Sea Drill. Proj._ 76, 403–407 (1983). CAS  Google Scholar  * de


Graaf, W., Wellsbury, P., Parkes, R. J. & Cappenberg, T. E. Comparison of acetate turnover in methanogenic and sulfate-reducing sediments by radio- and stable-isotope-labeling and


specific inhibitors: Evidence for isotopic exchange. _Appl. Environ. Microbiol._ 62, 772–777 (1996). CAS  PubMed  PubMed Central  Google Scholar  * Cragg, B. A._et al_. Bacterial profiles in


deep sediments of the Santa Barbara Basin Site 893. _Proc. ODP Sci. Res._ 146, 139–144 (1995). Google Scholar  * Cragg, B. A._et al_. The impact of fluid and gas venting on bacterial


populations and processes in sediments from the Cascadia Margin accretionary system (sites 888–892) and the geochemical consequences. _Proc. ODP Sci. Res._ 146, 399–411 (1995). CAS  Google


Scholar  * Furnes, H., Thorseth, I. H., Tumyr, O., Torsvik, T. & Fisk, M. R. Microbial activity in the alteration of glass from pillow lavas from Hole 896A. _Proc. ODP Sci. Res._ 148,


191–214 (1996). Google Scholar  * Giovannoni, S. J., Fisk, M. R., Mullins, T. D. & Furnes, H. Genetic evidence for endolithic microbial life colonising basaltic glass/seawater


interfaces. _Proc. ODP Sci. Res._ 148, 207–214 (1996). Google Scholar  * Rochelle, P. A., Fry, J. C., Parkes, R. J. & Weightman, A. J. DNA extraction for 16S rRNA gene analysis for


determining genetic diversity in deep sediment communities. _FEMS Microbiol. Lett._ 100, 59–66 (1992). Article  CAS  PubMed  Google Scholar  * Parkes, R. J._et al_. Biogeochemical processes


in gas hydrate zones. _Abstracts, Exploration and exploitation of non-living deep-sea marine resources._Challenger Society for Marine Science & Geological Society, Marine Studies


Group(Geological Society, London, (1996)). * Jørgensen, B. B., Isaksen, M. F. & Jannasch, H. W. Bacterial sulfate reduction above 100 °C in deep-sea hydrothermal sediments. _Science_


258, 1756–1757 (1992). Article  ADS  PubMed  Google Scholar  * Parkes, R. J. & Taylor, J. Analysis of volatile fatty acids by ion-exclusion chromatography, with special reference to


marine pore water. _Mar. Biol._ 77, 113–118 (1983). Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS We thank ODP for allowing us to obtain samples on Leg 164; T. Woodward


and I. Mather for their assistance with sample collection and initial handling in the laboratory; J. Maxwell, E. Shock and J. Whelan for comments on the original manuscript; P. Egeberg for


facilitating analysis of Site 997; M. Isaksen for details of the thermal gradient system, and F. Wheeler for its construction. This work was funded by the European Union Environment


Programme and the Natural Environment Research Council (UK). AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Geology, University of Bristol, Wills Memorial Building, Queens Road,


BS8 1RJ, Bristol, UK Peter Wellsbury, Kim Goodman, Barry A. Cragg, Stephen P. Barnes & R. John Parkes * Department of Chemistry, University of Bergen, Allegt, 41, N-5007, Bergen, Norway


Tanja Barth Authors * Peter Wellsbury View author publications You can also search for this author inPubMed Google Scholar * Kim Goodman View author publications You can also search for


this author inPubMed Google Scholar * Tanja Barth View author publications You can also search for this author inPubMed Google Scholar * Barry A. Cragg View author publications You can also


search for this author inPubMed Google Scholar * Stephen P. Barnes View author publications You can also search for this author inPubMed Google Scholar * R. John Parkes View author


publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to R. John Parkes. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS


ARTICLE CITE THIS ARTICLE Wellsbury, P., Goodman, K., Barth, T. _et al._ Deep marine biosphere fuelled by increasing organic matter availability during burial and heating. _Nature_ 388,


573–576 (1997). https://doi.org/10.1038/41544 Download citation * Received: 19 May 1997 * Accepted: 19 June 1997 * Issue Date: 07 August 1997 * DOI: https://doi.org/10.1038/41544 SHARE THIS


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